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Biol. Lett.
doi:10.1098/rsbl.2011.0489
Published online
Animal behaviour
A new navigational
mechanism mediated
by ant ocelli
Sebastian Schwarz1,*,†, Antoine Wystrach1,2,†
and Ken Cheng1
1
Department of Biological Sciences, Macquarie University,
Sydney, Australia
2
CRCA, Université Paul Sabatier, Toulouse, France
*Author for correspondence ([email protected]).
†
These authors contributed equally to the study.
Many animals rely on path integration for navigation and desert ants are the champions. On
leaving the nest, ants continuously integrate
their distance and direction of travel so that
they always know their current distance and
direction from the nest and can take a direct
path to home. Distance information originates
from a step-counter and directional information
is based on a celestial compass. So far, it has
been assumed that the directional information
obtained from ocelli contribute to a single
global path integrator, together with directional
information from the dorsal rim area (DRA) of
the compound eyes and distance information
from the step-counter. Here, we show that ocelli
mediate a distinct compass from that mediated
by the compound eyes. After travelling a two-leg
outbound route, untreated foragers headed
towards the nest direction, showing that both
legs of the route had been integrated. In contrast,
foragers with covered compound eyes but uncovered ocelli steered in the direction opposite to the
last leg of the outbound route. Our findings
suggest that, unlike the DRA, ocelli cannot by
themselves mediate path integration. Instead,
ocelli mediate a distinct directional system,
which buffers the most recent leg of a journey.
Keywords: ocelli; ants; navigation; path integration;
compound eyes; Melophorus bagoti
1. INTRODUCTION
To navigate in the world, insects are guided visually by
both celestial and terrestrial cues [1 –3]. Both compound eyes and the less conspicuous ocelli encode
visual information. Unlike compound eyes, ocelli do
not encode detailed image information [4– 6]. In
flying insects, it has been shown that ocelli stabilize
flight by quickly detecting changes of light intensities
in the dorsal visual hemisphere owing to sudden
deviations from a given flight attitude [4,5,7]. In
ground-based ant species, it is only known that ocelli
extract directional information from celestial compass
cues (e.g., polarized skylight, sun’s position), whereas
terrestrial compass information from surrounding
landmarks are not computed [6,8]. So far, it has
been assumed that such directional information
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2011.0489 or via http://rsbl.royalsocietypublishing.org.
Received 9 May 2011
Accepted 15 June 2011
obtained from ocelli contribute to a single global
path integrator together with directional information
from the compound eyes and distance information
from the step-counter [1,9]. By manipulating the
visual input of either the compound eyes or the ocelli
of the ant Melophorus bagoti, we found that ocelli mediate a second navigational mechanism separate from
the one mediated by the compound eyes.
2. MATERIAL AND METHODS
Data collection took place in Alice Springs, Northern Territory,
Australia. To ensure that the ants had access to celestial compass
cues [10], all experiments were conducted under clear or slightly
cloudy sky.
Ants were free to collect food items at the end of a straight or twoleg training route. The two segments of the two-leg route were 5.8 m
long and approximately 1.0 m wide and formed an angle of approximately 1408. White wooden planks, which were sunk into the ground
and stuck out approximately 0.10 m, enclosed the nest and the outbound route, thus preventing the ants from foraging elsewhere. The
‘walls’ were low enough to allow a view of the sky and the surrounding landscape. Foraging ants that reached the feeder on the training
field for the first time, and picked up a food item, were marked on the
abdomen with a daily colour of enamel paint. All marked ants were
able to dash between feeder and nest for at least one full day before
being tested. A test consisted of releasing the ant on an unfamiliar
test-field after one out of three painting treatments: either the eyes
(Oc), the ocelli (Ey) or the back of the head (Ct) were covered
with acrylic paint (figure 1a). The treatment itself had no noticeable
effect on the homing behaviour of the tested ants (electronic supplementary material, figure S2). Treated ants that picked up a
cookie crumb were transferred in the dark to the unfamiliar testfield approximately 60 m away from the training area. The unfamiliar
surrounding of the test-field ensured that the ants relied only on
celestial compass information for homing. A goniometer (diameter
1.2 m) with 24 sectors of 158 each was used to record the initial
headings of the ants at 0.6 m from the release point. After travelling
0.6 m, the tested ants tended to stay with their initial headings and
no switch in their homing direction appeared. The ants’ directional
choices were analysed with circular statistics [11].
3. RESULTS
In previously published results [6], we caught M.
bagoti foragers at a feeder after they had travelled a
straight outbound route. These so-called full vector
(FV) ants have information about distance and direction in order to integrate the shortest way home. We
released the FV ants with untreated compound eyes
but covered ocelli (figure 1a; Ey) onto an unfamiliar
test-field that ruled out the possible use of panoramic
cues. On the test-field, FV_Ey foragers headed straight
towards the (fictive) nest direction [6]. In this study,
we caught foragers after travelling a straight out- and
inbound route just before they entered the nest. Such
zero-vector (ZV) ants lack any distance and directional
information from the global path integrator. Surprisingly, when released on the test-field with covered
compound eyes and uncovered ocelli, these ants
(ZV_Oc) did not orient randomly, as the ZV of the
global path integration input would predict, but
headed significantly in the direction opposite to the
feeder-nest direction (figure 1b; V test: ZV_Oc11.53,
n ¼ 20, p , 0.001).
To examine the compass information obtained from
ocelli, we tested ants after they had travelled a two-leg
foraging route (figure 2). Foragers were caught at the
feeder, treated and released on the unfamiliar test-field.
Ants with covered ocelli (Ct; Ey) were significantly
oriented towards the (fictive) nest direction on the testfield (figure 2a; V test: Ct31.9, n ¼ 36, p , 0.001;
Ey21.3, n ¼ 30, p , 0.001; t-test: Ct21.6, p ¼ 0.12;
This journal is q 2011 The Royal Society
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2
S. Schwarz et al.
Ocelli navigation in ants
nest
(b)
(a)
10 m
Ct
control
Ey
covered ocelli
Oc
covered eyes
n = 20
ZV_Oc
feeder
Figure 1. (a) Different test conditions with sham painted control ants (Ct), ants with covered ocelli (Ey) and ants with covered
compound eyes (Oc). Control ants were painted on a region of the head that covered neither ocelli nor compound eyes.
(b) Directional choices of zero-vector (ZV) ants released on unfamiliar terrain with ocelli input only (Oc) after a straight outand inbound trip (route is not to scale). Circular histogram shows ants’ headings after travelling 0.6 m in sectors of 158. Black
arrow, mean vector of the distribution. Black arc, 95% confidence intervals. Black arrowhead, nest compass direction.
(a) nest
4.5 m
feeder
1st leg
5.8 m
2nd leg
5.8 m
n = 36
n = 31
n = 41
Ct
Ey
Oc
nest
(b)
10 m
covered
ocelli
n = 20
n = 47
Ey
Oc
feeder
Figure 2. Directional choices of treated ants released on unfamiliar terrain after a straight or two-leg outbound trip (routes are
not to scale). Circular histograms show the ants’ heading after travelling 0.6 m in sectors of 158. Black arrow, mean vector of the
distribution. Black arc, 95% confidence intervals. Black arrowhead, nest compass direction. Star, significant orientation (V test,
ps , 0.001). (a) Headings of ants released on unfamiliar terrain with both compound eyes and ocelli inputs (Ct), compound
eye input only (Ey) or ocelli input only (Oc). Grey arrowhead, compass direction opposite to the second leg of the outbound
route. (b) Headings of ants with covered ocelli during the straight outbound trip and released on unfamiliar terrain with
compound eyes input only (Ey) or ocelli input only (Oc).
Ey0.91, p ¼ 0.37). Ants with covered compound eyes but
functional ocelli (Oc), however, did not run towards the
nest direction (t-test: Oc21.57, p , 0.001). They chose
the direction opposite to the second, last leg of
the outbound route (figure 2a; V test: Oc17.8, n ¼ 41,
p ¼ 0.001; t-test against second leg direction: Oc20.66,
p ¼ 0.52; Ct8.37, p , 0.001; Ey6.25, p , 0.001). The
headings of Oc foragers differed significantly from those
of Ey (Watson-Williams test, F ¼ 21.4 p , 0.001) and
Ct ants (Watson-Williams test, F ¼ 17.0 p , 0.001).
To show that ocelli mediate a distinct compass
mechanism, it is necessary to confirm that the directional information derived from the dorsal rim area
(DRA) is not accessible via the ocelli. To test this, we
captured ants at the feeder that had just run a straight
outbound trip with covered ocelli (Ey) and tested them
either with unchanged (Ey) or reversed (Oc)
Biol. Lett.
conditions (figure 2b). Ey ants showed no difficulties
in heading home (V test: Ey14.20, n ¼ 20, p , 0.001),
but Oc foragers displayed random directional choices
(figure 2b; V test: Oc7.68, n ¼ 47, p ¼ 0.06). The directional information encoded by the DRA is not
transferred to the compass to which the ocelli contribute, supporting the hypothesis of two distinct
compasses. The random directional choices of Oc
ants could be also due to the unlikely possibility that
ocelli might not be functional for several minutes
after the removal of the paint.
4. DISCUSSION
After travelling a two-leg foraging route, ants on an
unfamiliar test-field with covered compound eyes but
open ocelli (figure 2a; Oc) did not compute direction
Downloaded from http://rsbl.royalsocietypublishing.org/ on April 19, 2017
Ocelli navigation in ants
and distance towards the nest; instead these ants
headed in a direction opposite to the last leg of
travel. These results are consistent with the behaviour
of the ZV ants with covered eyes but functional ocelli
(figure 1b; ZV_Oc), heading opposite to the home
direction that was the direction of the last leg of
travel. The directional information mediated by the
DRA of the compound eyes appears to be inaccessible
to ocelli (figure 2b). This suggests the presence of two
distinct mechanisms. The DRA provides directional
information to the global path integrator—which
keeps track of the nest position—whereas ocelli
supply directional information to a distinct mechanism—which buffers the most recent leg of travel and
overrides previous information (electronic supplementary material, figure S1b). Then what could be the
function of the additional directional compass driven
by the ocelli? Ant ocelli might act as a supporting
system for the global path integrator mediated by the
compound eyes. However, foragers with continuously
covered ocelli during the two-leg outbound route,
headed solidly in the direction of the fictive nest
when released on the test-field (electronic supplementary material, figure S1a). Therefore, ocelli are not
necessary for global path integration.
It could be assumed that the function of ant ocelli
resembles that of flying insects in supplying a means of
maintaining and controlling direction and body orientation through a variety of cues (e.g., horizon, image
motion, sun). However, we know that the homing
paths of ants with covered compound eyes and uncovered ocelli (Oc) are fairly tortuous and not as
accurately oriented as those of ants with compound
eyes only (Ey). In fact, Oc ants’ homing paths were
almost as tortuous as paths of totally blinded ants [6].
Therefore, it seems that the maintenance and stabilization of the homing paths in walking ants are mediated
by the compound eyes and not the ocelli. Another
explanation is thus required.
Melophorus bagoti foragers follow visually guided
idiosyncratic routes through a cluttered environment
[12]. Sometimes, a newly appeared obstacle or the
presence of aggressive conspecifics from other colonies
may force the forager to leave her familiar route,
ending up in unfamiliar surroundings. In such cases,
the ocelli-driven compass could possibly allow the
ant to return to her well-known route rather than
homing towards the nest through unknown terrain.
The discovery of this distinct navigational mechanism
mediated by the ocelli also raises mechanistic and evolutionary questions. Ocelli are known for their fast
neurological response [5] and it may be advantageous
to process directional information independently.
The directional information encoded by the ocelli
appears indeed to be processed separately from that
derived from the compound eyes, but what about the
odometric information? Is the ocelli-mediated compass
processed together with the step-counter that is also
used for the global path integrator, or is it processed
with another odometric cue such as optic flow or
encoded only as a direction without odometric information? Interestingly, in many ant species ocelli are
seldom found in workers but often present in winged
Biol. Lett.
S. Schwarz et al.
3
alates [13] and other flying insects [7]. Therefore,
the ocelli-driven compass might be just an exaptation
derived from flying ancestors or flying reproductive
alates. Conversely, the question of whether the ocelli
of alates are used for some directional purpose, as
they are by the foragers in this study, or merely for
flight and gaze stabilization as in other flying insects
[4,7], remains to be investigated.
In summary, our results demonstrated that ocelli
could not by themselves mediate path integration in
ground-based insects. Such a discovery, with its
associated mechanistic, functional and evolutionary
questions, reminds us how complex, flexible and welladapted the structure underlying insect navigation is.
We thank CSIRO and CAT, Alice Springs for providing
facilities. We appreciate the assistance of Laurence Albert
in data collection and thank Paul Graham for comments on
the manuscript. The work was funded by graduate
scholarships of Macquarie University and a Discovery
Grant from the Australian Research Council (DP0770300).
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